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Study protocol for a cluster-randomized trial to compare human papillomavirus based cervical cancer screening in community-health campaigns versus health facilities in western Kenya

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Despite guidelines for cervical cancer prevention in low-resource countries, a very small proportion of women in these settings undergo screening, and even fewer women are successfully treated. Using pilot data from western Kenya and World Health Organization recommendations, we developed a protocol to implement evidence-based cervical cancer screening and linkage to treatment strategies to the rural communities.

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S T U D Y P R O T O C O L Open Access

Study protocol for a cluster-randomized

trial to compare human papillomavirus

based cervical cancer screening in

community-health campaigns versus health

facilities in western Kenya

Megan J Huchko1*, James G Kahn2, Jennifer S Smith3, Robert A Hiatt2, Craig R Cohen4and Elizabeth Bukusi5,6

Abstract

Background: Despite guidelines for cervical cancer prevention in low-resource countries, a very small proportion of women in these settings undergo screening, and even fewer women are successfully treated Using pilot data from western Kenya and World Health Organization recommendations, we developed a protocol to implement

evidence-based cervical cancer screening and linkage to treatment strategies to the rural communities We describe the protocol for a cluster-randomized trial to compare two implementation strategies for human-papillomavirus (HPV)-based cervical cancer screening program using metrics described in the RE-AIM (reach, efficacy, adaption, implementation and maintenance) framework

Methods: The study is a three-year, two-phase cluster-randomized trial in 18 communities in western Kenya During Phase 1, six control communities were offered screening in health facilities; and six intervention communities were offered screening in community health campaigns Screening was done with human-papillomavirus testing

through self-collected specimens Phase 1 ended and we are working in partnership with communities to further contextualize the implementation strategy for screening, and develop an enhanced linkage to treatment plan This plan will be tested in an additional six communities in Phase 2 (enhanced intervention) We will compare the reach, efficacy, cost-effectiveness and adaptability of the implementation strategies

Discussion: Effective low-cost cervical cancer prevention technologies are becoming more widely available in low- and middle-income countries Despite increasing government support for cervical cancer prevention, there remains a sizeable gap in service availability We will use implementation science to identify the most effective strategies to fill this gap through development of context-specific evidence-based solutions This protocol design and results can help guide implementation of cervical cancer screening in similar settings, where women are most underserved and at highest risk for disease

Trial registration: This trial is registered at ClinicalTrials.gov, NCT02124252

Keywords: Cervical cancer screening, Community health campaigns, Kenya, HPV self-collection, Implementation science

* Correspondence: megan.huchko@duke.edu

1 Duke University, Global Health Institute and Department of Obstetrics and

Gynecology, 310 Trent Drive, Room 204, Durham, NC 27708, USA

Full list of author information is available at the end of the article

© The Author(s) 2017 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made The Creative Commons Public Domain Dedication waiver

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Despite the fact that cervical cancer is highly preventable

through vaccination and organized screening programs,

over 500,000 women worldwide are diagnosed with the

disease every year [1] About 9 out of 10 cervical cancer

deaths occur in low-resource countries, with a particularly

high burden in sub-Saharan Africa, where the mortality

rate is 85% [2, 3] The inequality between high and

low-resource countries is mainly due to lack of screening in

low-resource countries, which lack the health care

infra-structure required for the cytology-based screening

pro-grams that have dramatically reduced the disease burden

in wealthier countries The World Health Organization

(WHO) recommends alternative cervical cancer

preven-tion techniques and protocols for low-resource countries

that employ low-cost or simple-to-use screening

technolo-gies [4] One such strategy– high-risk human

papilloma-virus (HPV) testing– has been shown to reduce the

incidence and mortality from cervical cancer when

coupled with outpatient treatment for women with

HPV-positive results [5]

In addition to effective screening tools, the impact of

cervical cancer prevention programs depends on two

main context-specific factors: (1) women’s access to

screening and (2) successful acquisition of treatment for

women who screen positive Access to both screening

and treatment is most challenging in poor rural areas,

due to geographic and infrastructure constraints [6, 7]

Most health care in rural areas takes place in small

health facilities with limited space, staffing, and

equip-ment, making it challenging to implement same-day

“screen & treat” strategies that have been proposed to

overcome barriers to treatment access [8] So, despite

the development of guidelines for cervical cancer

screen-ing that employed evidence-based technologies and

lower resource protocols, the lack of rigorously tested,

context-specific implementation strategies has left a gap

between policy and practice

In order to develop a context-specific, sustainable

im-plementation strategy, we undertook formative work to

identify local barriers and facilitators for cervical cancer

screening in government-supported health facilities in

rural western Kenya, an area of East Africa with a high

cervical cancer burden and screening rates as low as 3%

[9, 10] We found that access to screening was limited

by lapses in service availability and lack of clinic

attend-ance for preventive care [11] When services were

avail-able, both providers and patients found the need for a

pelvic exam limited the acceptability of cervical cancer

screening Based on the facility-based barriers, we

devel-oped and piloted a highly successful community health

campaign model for screening, consisting of outreach

followed by a brief campaign held in a central site in the

community, offering on-site screening and referrals for

treatment [12] An advantage of community-based screening is that only screen-positive women need to visit health facilities for follow-up care, reducing the visit burden for both woman and facilities, and allowing resources to be directed toward strategies to increase treatment uptake, such as intensified follow-up, trans-portation assistance or mobile units that bring treatment

to remote villages Thus, as has been seen in other health services [13–15], by combining community-screening with enhanced linkage strategies, our approach could maximize the health impact by increasing the number of women screening and the proportion successfully accessing treatment

To address the reluctance around pelvic exams, we chose to offer screening with self-collected specimens for HPV testing, an evidence-based strategy that would eliminate pelvic exams for initial screening, further increasing screening acceptance and efficiency We developed a study protocol that will allow us to compare two context-specific implementation strategies for an HPV-based cervical cancer prevention program through

a cluster-randomized trial of HPV-based cervical cancer screening in community-health campaigns versus health facilities using the RE-AIM framework [16, 17] This paper describes the study protocol (V 3.0, 20 July 2017) and the plan to evaluate the adaptability, comparative ef-fectiveness and cost-efef-fectiveness of these two strategies Methods

Study design and setting

The study is a two-phase cluster randomized trial in western Kenya to evaluate reach, effectiveness, cost-effectiveness and maintenance of two implementation strategies for a cervical cancer prevention protocol that consists of four critical, evidence-based components:

(1).HPV and cervical cancer outreach and education.In western Kenya, we found that women’s baseline knowledge and perception of cervical cancer risk is low; a brief educational intervention provided

by community health workers in primary care clinics improved these baseline factors and increased women’s intention to screen [18]

(2).HPV-testing using self-collected specimens with referral for treatment based on a single positive result.An HPV-based screening strategy is effective at reducing incidence of cervical pre-cancer and invasive cancer when women with screen-positive results undergo cryotherapy [5,19,20] Self-collected specimens are highly accurate, with comparable results

to provider-collection for the detection of high-grade cervical precancer [21–23] Women have consistently found self-sampling acceptable and preferable to provider-testing [24–26]; this finding has been

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supported in studies from sub-Saharan Africa [27,28].

Studies in various countries have shown that a

self-collection strategy increases screening uptake by

women not attending clinics [29–34]

(3).Notification of screening results using text

messaging.Based on our prior experience with

mobile health interventions [35,36] and the high

rates of cell phone use in western Kenya [37], HPV

test results were sent to all women via text message

with instructions about appropriate follow-up as

recommended by the Kenya Ministry of Health

guidelines

(4).Treatment with cryotherapy unless

contraindicated by cervical exam.Cryotherapy is a

low-cost, effective treatment method that can be safely

carried out by mid-level providers in low-resource

settings [38,39] Women who are not candidates for

cryotherapy (i.e lesions too large or abnormal cervical

anatomy) were offered Loop Electrosurgical Excision

Procedure carried out in the County Hospital

Together, HPV testing followed by cryotherapy for

women who test positive reflect the current WHO

recommendations [40]

In Phase 1 of this study, we compared two

implemen-tation strategies that incorporated these four

evidence-based elements of screening Based on our preliminary

data, we found that reaching and attending a health

facility for preventive care was a significant barrier to

screening for many women Therefore, the main

object-ive was to compare a model offering screening in brief,

high throughput community health campaigns to that of

a standard of care in which screening was offered in

local health facilities using the metrics defined in the

modified RE-AIM framework

In Fig 1, we present an overall schema of the

cluster-randomized trial In Phase 1, six communities were

ran-domized to the intervention: HPV screening carried out

in community health campaigns The remaining six

were comparison communities: HPV testing offered in government health facilities HPV-test positive women

in all communities were referred to the County hospital for immediate treatment, which is considered standard linkage to treatment

Development of an enhanced strategy for linkage to treatment: After Phase 1, we have an “phase inter-vention development” period in which we are evaluating the results from the trial The outcomes from the quali-tative and quantiquali-tative measures will be used to refine the screening intervention using context-specific details and develop an enhanced strategy for linkage to treat-ment Although we have identified factors that enable and inhibit women’s access to treatment, we chose to wait until after Phase 1 for the development of the enhanced strategy for linkage to treatment in order to truly work in partnership with the community The de-layed development of the linkage to treatment strategy has allowed us obtain a baseline measure of the efficacy

of standard referrals and identify factors that would in-fluence women’s access to care in this setting

After developing the strategy for enhanced linkage, we will pilot and then test the linkage to treatment strategy

as part of an“enhanced intervention” in the six commu-nities that served as controls in Phase 1 Using these communities for the enhanced intervention increases the efficiency of the study in two ways: i we will have done community enumeration and engagement, and ii

we will compare linkage to treatment outcomes from these “enhanced intervention” communities to the inter-vention communities from Phase 1

Study activities Study preparation

 Community enumeration and randomization: Prior to the initiation of the cluster randomized trial, we characterized the study communities using

a combination of census data, health facility

Fig 1 Two-phase cluster-randomized trial design

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information, mapping and prospective demographic

data We identified communities of approximately

7500 people in three sub-counties of Migori County

in western Kenya (population: 350,000, 65

govern-ment health facilities) Population estimates were

calculated using the 2009 Kenyan census data with

population growth estimates for 2015 and 2014, a

method that was validated through door-to-door

enumeration for a recent large-scale community

randomized trial in rural western Kenya [41]

Eligible communities had at least one government

health facility with capacity to provide HPV testing,

support from community leaders for the community

outreach and/or health campaigns, accessibility to

health centers via a maintained transportation route

and sufficient distance from other potential study

sites to limit contamination between arms (buffer

zones) As our target group is women in rural

communities, we excluded urban settings or

communities in which the nearest health center is

Migori County Hospital and those that were taking

part in a cluster-randomized trial of large-scale

community-health campaigns for HIV-testing [41]

We conducted unmatched randomization using a

random number generator on Stata 10 The

unmatched design will allow us to consider the

relationship between community-level factors and

our outcomes of interest After communities were

chosen, population estimates were refined through

household enumeration done by community health

workers assigned to villages and sub-locations within

the communities

 Provider and key stakeholder focus groups:

Clinicians and community health workers

(“providers”) within the community health

campaigns and health facilities participated in focus

group discussions to provide baseline data about

perceived barriers and strategies to facilitate HPV

screening uptake during the planning and

implementation adaptation period of the study

Although we sought key stakeholder input

throughout the development of the implementation

strategies, we held three focus group discussions

with key stakeholders in the intervention and

control communities for Phase 1 (community chiefs,

leaders of women’s groups, reproductive health

coordinator, medical superintendent and Charge

Nurse of Migori District Hospital) The goals of

these focus groups were to obtain a group

perspective on the intervention as planned for their

communities, any anticipated challenges and

strategies to optimize the screening strategy in both

arms Focus group discussions were analyzed using

the theoretical domains framework, which mapped

behaviors to intervention strategies, using evidence-based principles of behavior change [42]

 Training and finalization of the screening protocol.We used educational modules piloted in western Kenya to provide standardized training in cervical cancer counseling and HPV-self testing to community health workers and clinicians [43] The community health workers received training in community outreach messaging, delivery of the educational module in the community health campaign setting, and teaching women how to perform self-collection of HPV specimens In addition to the general training, clinicians had undergone Ministry of Health-supported training to learn the cervical cancer screening protocol, including follow-up and pre-treatment exams Two nurses who had undergone cryotherapy training were identified and supervised for ten cryotherapies

at the County Hospital prior to study initiation

Cluster randomized trial: Phase 1

After community enumeration, training and protocol finalization, we launched the cluster-randomized trial in the six control and six intervention communities in Migori County (Figure 2) Phase 1 of the trial, consisting

of the activities listed below, took place over the course

of 1 year

 Outreach and education:In all communities, information about cervical cancer screening and the opportunity to learn more about HPV-based testing were provided through community outreach, including fliers, posters and brief informational sessions in markets, churches and women’s group meetings Women and community leaders were provided with information on how to access cervical cancer screening in their community, e.g location of clinic or timing and location of community health campaign In all communities, women were invited

to participate in a brief, standardized cervical cancer education module, either at the health campaign or

in the health facility The module is approximately

15 min and covers topics ranging from simple anatomy, definition of cervical cancer and HPV, how screening works, what treatment is available for precancerous lesions, and how to perform HPV self-testing

 Community-based testing (intervention group):

In six communities randomized to community-based HPV testing, community outreach teams carried out two-week community health campaigns in which HPV-testing was offered through self-collection In order to reach the entire community, the campaign moved to multiple sites over the two-week period,

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with approximately one to 2 days at each site The

campaigns consisted of health education and informed

consent, after which a health worker provided

additional instructions about self-collection and

recorded a mobile phone number before dispensing

the HPV testing kit The woman then would go to a

private area in the campaign tent to self-collect the

specimen and returned the completed collection kit to

the health worker prior to leaving

 Clinic-based testing (comparison group):In the

six communities randomized to the control arm

(clinic-based testing), women were directed through

community outreach to go to their local health facility

during regular clinic hours to carry out screening At

the clinic, a health worker offered the educational

module, obtained informed consent and provided

additional information about self-collection, and

recorded a mobile phone number before dispensing

the HPV testing kit and instructions

 HPV testing:While HPV test results are not the

primary outcome for this study, the accuracy and

reproducibility of measurements are essential for

outcomes in both arms and for modeling the impact

of the implementation strategies in larger populations We tested the DNA for 14 HPV types (16, 18, 32, 33, 35, 39, 45, 51, 52, 56, 58, 59 and 68) using CareHPV™ testing system Collected

specimens were transported daily from the CHCs and weekly from the health facilities to the study lab

at Migori County Hospital Tests were run in batches of 90, with a turnover time of approximately

1–2 weeks for results

 Notification of HPV results:HPV test results were preferentially sent to women via text message with instructions about appropriate follow-up as recommended by the Kenya Ministry of Health guidelines Messages were developed by key stakeholders and women from the target population during the focus group discussions Women who did not have access to a phone, or did not wish to receive their results by SMS could opt for a return visit to the clinic, or a home visit

 Standard referral for treatment (both arms, Phase 1):Women who were HPV-positive were

Fig 2 Map of communities randomized to control and intervention activities in Migori, County Kenya This map was developed by Easter Olwanda, who has provided written permission for use in this publication

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referred to Migori County Hospital for a visual exam

with acetic acid and treatment with cryotherapy per

the WHO guidelines [44]

 In-depth participant interviews and focus

groups:We conducted semi-structured interviews

with randomly selected participants in both arms at

three key points in the cervical cancer prevention

cascade: screening delivery (n = 30), notification of

results (n = 30) and treatment access (all) Participants

were contacted either in person or by phone, and

interviews conducted in person by experienced

qualitative interviewers in the local language using

interview guides developed by the research team

Topics explored in these interviews will elucidate ways

to make cervical cancer screening more acceptable and

accessible to women Interviews captured quantitative

data about women’s participation in various aspects of

the prevention cascade Interviewers then explored

women’s perspectives of their experience with the

intervention and explanatory factors related to the

decisions to access screening and treatment through

open-ended questions Among women who did not

access treatment, we probed for factors or strategies

that would allow them to link to care in the future

 Provider and key stakeholder interviews and

focus groups:During the cluster- randomized trial,

providers in the community health campaigns

underwent brief interviews at two time points: after

three and six campaigns had been completed In the

clinic-arm, providers underwent interviews at three,

6 and 12 months into the intervention These

interviews will help to understand explanatory

factors for the success or failure of the intervention

from a health system perspective Interview topics

included personal attitudes and beliefs around

screening importance and feasibility, perceived and

actual barriers to implementation and potential

strategies to overcome provider, health delivery and

patient-level barriers to screening and treatment

Intervention development and cluster randomized trial:

Phase 2

 Enhanced linkage to treatment:We will work

with health care providers, community members

and other stakeholders to review outcomes from the

quantitative, qualitative and process measures in

Phase 1, critically examine and modify the cervical

cancer screening strategy to develop and pilot the

enhanced linkage to treatment intervention over a

6–9 month period between Phase 1 and 2 We will

do this through a series of key stakeholder meetings,

followed by the establishment of smaller working

groups for the creation of the specific intervention

components In the first set of meetings, we will present the findings from Phase 1 and seek feedback

on representativeness and discuss implications for culturally relevant intervention strategies Options for the most feasible and acceptable strategies to increase the number of women linking to treatment will be explored in the light of that data

Criteria for potential strategies include: community-developed, low-cost, feasible in all study communities, and able to ensure treatment for HPV-positive women

in a timely manner in accordance with Ministry of Health guidelines In a second, small stakeholder meet-ing, we will review potential strategies discussed and developed in the first meeting, and discuss solutions proposed in other settings, including the use of mobile treatment units, transportation vouchers, and treatment

“navigators” to help women understand and travel to treatment sites Once the linkage intervention has been defined, we will hold another working group with stake-holders to create a standardized protocol, training man-ual, standard operating procedures and data collection instruments After equipment procurement, provider training and further outreach messaging, the enhanced linkage strategy will be piloted in two to three Phase 1 intervention communities prior to launch of Phase 2

Implementation framework

The study design, and outcome measures are centered

in the essential implementation metrics as defined by the RE-AIM framework, which modified to the context

of our study (Table 1) [17] Outcomes will be evaluated through quantitative, qualitative and process measures This design will allow us to test the following hypotheses:

 Community-based cervical cancer screening will reach a larger portion of eligible women and be more acceptable to patients and providers than clinic-based testing (REACH)

 A community-driven intervention will improve linkage to treatment among women who need treatment after an HPV-positive screening test compared to standard referral (EFFICACY)

 We will identify modifiable patient and health system challenges that can be addressed to make health campaign based HPV testing and enhanced linkage to treatment succeed and be sustainable (ADOPTION & MAINTENANCE)

 Community-based cervical cancer screening with enhanced linkage to treatment will have a greater population-level health impact as measured in women reached with screening and any necessary treatment, and favorable cost-effectiveness profile

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compared to clinic-based strategies and standard

referral for treatment (IMPLEMENTATION)

Participants

Our target population is women living in rural Kenya

who are eligible for and would benefit from cervical

can-cer screening per the Kenya Ministry of Health

Guide-lines (25–65 years old with an intact uterus and cervix)

The study population is women 25–65 years in the

twelve communities in the Nyanza Province who access

screening during both phases of the trial

Recruitment and consent

Communities participating in the trial provided verbal

assent in the planning process with written consent

ob-tained from individuals for screening Participants were

recruited through the community health campaigns and

in the clinics Women within the target age range were

invited to attend the cervical cancer educational module

After the health talk, women were asked to provide

in-formed consent by research assistants for a post-module

questionnaire and follow-up after screening completion

Women who were not willing to provide informed

con-sent were still able to attend the health talk and have

ac-cess to the HPV screening strategy assigned to her arm,

but were not contacted for the follow-up in-depth

inter-views or participation in focus group discussions

Primary and secondary endpoints

To determine the reach of cervical cancer screening

using HPV-testing in community health campaigns

compared to clinics, we are using the following metrics: i) the absolute number of women who completed screening in each arm and ii) the proportion of women

in each arm who completed screening The total number

of women in each arm is the number of women 25–65

in each community as determined by census data Secondary outcomes will include iii) the proportion of women who accept screening among women offered at each site and iv) the proportion of women in the clinic-based arm who request clinician-collected specimens

To determine the efficacy of a community-developed strategy to increase treatment access, we will compare the efficacy of the community-based HPV testing with standard versus enhanced linkage to treatment using the following metrics: i) the number of women who receive treatment after screening HPV + in the intervention (Phase 1) compared to the enhanced intervention (Phase 2) and ii) the proportion of HPV-positive women in each arm who complete treatment Secondary outcomes that address quality of care concerns for the models will include iii) the proportion of women who receive the correct treatment (per Ministry of Health protocol) during a single treatment visit and iv) the average time between HPV testing and access of treatment by arm

Data collection

We collected data on both screening and linkage to treatment from both control and intervention communi-ties in Phase 1 Data was collected by members of the research team and entered into pre-programmed tablet computers using OpenDataKit software (ODK™),(https://

Table 1 A modified RE-AIM framework to evaluate community health campaign-based cervical cancer screening compared to health-facility based screening

women in rural kenya?

A screening strategy offered through community health campaigns in a central location will reach a large proportion of reproductive-aged women How do we reach them?

Effectiveness Is the program effective? Are women getting screened for

cervical cancer with HPV?

A community-based strategy allowing for self-testing will be highly acceptable.

How do we ensure effectiveness? Are HPV + women successfully

linking to treatment?

Innovative, patient and provider-designed strategies will increase the number of women linking to care.

Adoption and

Maintenance

How can strategy be maintained

after initial implementation and

adopted in similar communities?

What are the patient, provider and delivery system processes necessary to ensure consistent service provision?

A screening protocol with a simple, patient-performed test offered as part

of a health fair will minimize the costs to the health care system to introduce screening What are the short and long-term

health effects in the community?

What is the population-level health impact

of screening using HPV self-testing in the CHCs with enhanced linkage to care?

The high number of at -risk women reached through the CHC-base strategy with enhanced linkage to care would produce a greater population-level health impact.

Implementation What is adherence to the

implementation strategy at

the delivery level?

Is HPV testing being offered and delivered consistently at the CHC and clinic sites?

Providing testing in a high-volume CHC will reach

a large number of women with low staffing and infrastructure needs, and will therefore have a lower cost per woman treated than a standard strategy.

What are the costs of

implementation?

What is the cost per lesion treated?

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opendatakit.org) which had been used by this research

team for the past several years Programming included

checks for range, structure, and internal consistency

During the community-health campaigns, data was

col-lected directly from providers and participants into the

tablets and was transferred daily via a secure electronic

transfer to our data center facility in Kisumu, Kenya and

stored on a secure server To capture visits and

out-comes from clinic-based screening and facility

treat-ment, a member of the research team visited each

clinical facility on a weekly basis to enter data from

Min-istry of Health registers and study-specific forms into

the tablets Data transfer from clinical-sites took place

weekly The same data collection procedures will be

ap-plied in Phase 2

Implementation consistency

All four basic components of the intervention (outreach/

education, HPV-testing, notification of results and

linkage to treatment) were monitored throughout Phase

I of the trial to ensure maintained fidelity to the protocol

and quality of service and message delivery Quantitative

outcome measures, as well as the process measures

listed below assessed continued fidelity of the

interven-tion as offered Qualitative data from in-depth

inter-views, focus-group discussions and process measures

will provide a more complete picture about subtle but

important factors that may influence the actual service

delivery and uptake

Sample size

Using estimates from the 2009 Kenya census [45] with

projected population growth for 2015 and results from

recent community-wide census enumeration carried out

by a cluster randomized trial in an adjacent district [46],

we have estimated the total available population of

women to be approximately 1000 per community of

5000 The estimates for attendance at community health

campaigns (60% or 600 women) and clinics (30% or 300

women) and screening uptake were based on our

forma-tive work, community health campaign attendance in

adjacent districts, and prior studies of self-collected

HPV testing [27, 28, 47] Our assumptions were that (1)

attendance would be higher at community health

cam-paigns and (2) screening uptake would be higher among

women attending community health campaigns because

most women attend based on outreach messaging

around cervical cancer These assumptions suggested a

study population of 510 women per community

acces-sing testing through community health campaigns and

210 accessing screening through clinics For Phase 1, the

total number of women accessing screening in the six

communities randomized to community health

campaigns would be 3060 and 1260 in communities

randomized to clinic-based testing We used these conservative estimates for sample size calculations (see below), but allocated resources for up to 4500 women in the community-testing arm and 2000 women in the clinic-based screening arm to ensure continuity of study activities We also enrolled all providers and targeted key ministry of health stakeholders for quantitative and qualitative assessments of barriers and facilitators to care A representative subset of this group were invited

to participate in meetings to develop the enhanced linkage intervention

Statistical analysis

 Preliminary Analysis:For each outcome, we will produce descriptive statistics (frequencies, proportions, etc.) overall, across clusters of interest (community, clinic, provider, etc.), and over time

We will also graph these data to identify visual trends

 Primary and Secondary Analysis:Although this is a community-level intervention, the main outcomes will be analyzed at the individual level We will compare the number and proportion of women who screen for HPV (reach) and who get treated for a positive HPV test (efficacy) in communities assigned

to community vs clinic-based testing using generalized estimating equations to account for the correlation among observations within communities Efficacy: We will employ a log link and Poisson distribution with an offset term to represent the size

of each community

 Power calculations:We anticipate being able to observe a 30% difference in overall screening uptake between the control and intervention arms, a conservative estimate relative to previous cluster randomized trials The power calculations assume an alpha of 0.05, a beta of 0.20, and an intracluster correlation coefficient of 0.072 for screening and 0.11 for treatment, based on calculations from a cluster-randomized trial of HPV efficacy [5]

Cost-effectiveness analysis (maintenance)

We assessed the costs, population health impact, and incremental cost effectiveness of three intervention strat-egies (clinic-based screening with standard linkage to treatment; community screening with standard linkage; and will assess community screening with enhanced linkage) To do this, we undertook a micro-costing of the resources needed to carry out the activities in both arms in Phase 1 and 2 Costing included 1) personnel (including fringe benefits); 2) recurring supplies and services; 3) capital and equipment; and 4) facility space Intervention costs were assessed using a uniform cost

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data collection protocol to quantify resources used and

associated costs in each of the study sites

(community-health campaigns, clinics, laboratories and district

hospi-tals) Data was obtained through administrative record

review and interviews with administrative, finance and

human resources staff, supplemented by direct

observa-tion in a limited number of staff “time and motion”

studies in order to distinguish cervical cancer-related

activities from other health services delivered by the

same personnel Costs were summarized as total

program costs as well as costs per woman screened and

per HPV positive women treated

We observed study outcomes to estimate the health

outcomes associated with each screening and linkage

strategy Observed data include will include the number

of women screened and treated for high-risk HPV, the

proportion of women undergoing cryotherapy vs LEEP,

and the side effects associated with each treatment We

will find the best possible available data to estimate the

prevalence of various HPV-subtypes in the region, and

the associated risks of cervical intraepithelial neoplasia

(CIN), recurrence rates of CIN after treatment, and

inva-sive cancer in women with and without treatment We

will translate each health event into a standard metric of

burden of disease, Disability-Adjusted Life Years

(DALYs), which combines morbidity (and associated

disability) with premature mortality (lost“life years”)

We will use the micro-costing described above to

esti-mate several indices comparing costs to desired program

outcomes: cost per case of HPV detected; cost per case

of CIN detected; cost per woman successfully linked to

facilities for treatment; and cost per woman treated We

will construct a decision model to estimate the health

impact of HPV screening and linkage to treatment in a

population cohort of 1000 women This model will

explicitly portray the paths from HPV to detection (by

clinical presentation or screening), the risks of clinical

progression, and outcomes with and without treatment

(early or late) It will incorporate data on local

epidemi-ology (HPV prevalence and cervical cancer, from Phase

1 and existing surveillance data); the clinical course of

HPV and cervical cancer (from scientific literature); and

the effectiveness of treatment (with cryotherapy and LEEP,

as well as for more advanced disease, from scientific

literature) Model outcomes will include deaths from

cervical cancer, lost years of life, and morbidity (short and

long-term), and DALYs (disability adjusted life years)

We will use the decision-analysis model to assess the

incremental cost-effectiveness ratio (ICER), defined as

the added cost per DALY averted, when comparing

intervention strategies We will also calculate the ICER

compared to the current standard, which is no organized

available screening, using baseline data of screening

availability and use to calculate this We will also

estimate the costs for scaled-up replication, which will include variations in the number of and costs for personnel, community-health campaign structure and duration, HPV screening test costs laboratory costs and different linkage strategies

Process measures

We will use quantitative process analyses to evaluate the strategy implemented in both arms at four levels of the intervention delivery process (Fig 3) These include a) the proportion of women from each community health campaign offered HPV testing or referral (community health campaign-level processes); b) the proportion of HPV tests for which valid results are available (specimen transport and laboratory processes); c) the proportion of women who receive their test results (community health worker processes); and c) the proportion of HPV+ women attending a treatment visit who receive the appropriate treatment per Kenya Ministry of Health guidelines (health delivery center processes) We will use data from the provider and participant interviews and focus groups to explore the factors impacting the relevant service delivery processes that affect the overall result though quantitative and qualitative measures as well as explore additional key barriers and facilitators to both screening and treatment Focus group data will enrich these conclusions and be used to develop an enhanced linkage intervention

Ethical review

The trial was reviewed by an implementation and dissemination science section at the National Cancer Institute prior to funding Ethical approval was obtained

by the Committee for Human Research at the University

of California, San Francisco (#14–13,698), Duke University Institutional Review Board (Pro0007742), and the Scientific and Ethical Review Unit at the Kenya Medical Research Institute (SERU 2918) Any major protocol changes will be communicated to all three review boards and to the trial registry at ClinicalTrials.gov Complete trial registry data is available in a Additional file 1

Trial status

Focus Group Discussions and in-depth interviews with key informants took place in August and September

2015 A pilot campaign took place in December 2015 Screening activities and enrollment in Phase I of the cluster-randomized trial were carried out between January and September 2016 We are now sharing feedback

of Phase I results and observations with various stake-holders (community members, health care providers, and health management teams) in preparation for FGDs and working groups, which are aimed at enabling us design a strategy for enhanced linkage to treatment

Trang 10

Substantial progress toward cervical cancer prevention

has been made through research validating low-cost

screening strategies that have been included in national

and international protocols and guidelines However, like

many international guidelines, the WHO cervical cancer

guidelines lacks advice on active implementation

strat-egies [48] While this is partly due to an emphasis on

the clinical portion of the guidelines, some of this can be

attributed to the lack of effective implementation

strat-egies Our goal with this novel study is to work with the

community using a rigorous implementation framework

to develop a strategy that could be scaled to improve

the reach and efficacy of cervical cancer prevention

programs in rural Africa, where the lack of health

care infrastructure and services has lead to poor

health outcomes We are also hoping that the

meth-odology of this project can be expanded to develop

implementation strategies that would help address

other health care needs

Based on our formative work, we expect that

community-based cervical cancer screening will reach a

substantially larger portion of eligible women than

clinic-based testing Our findings will help guide

imple-mentation and optimization of a community-based HPV

testing model While we anticipate that the

community-driven enhanced intervention will be more effective at

link-ing women to facilities for treatment than the standard

re-ferral system, this study will allow us to test both models

and look at various aspects of implementation, including

cost-effectiveness In addition to these findings, we will

provide a model for a successful strategy to link women to

treatment within cervical cancer screening program and to

provide program leaders and policymakers with a tool kit

to design and evaluate a context-specific enhanced linkage

strategy that could be implemented in their own settings

We expect that community-based HPV screening will have

a greater cost effectiveness and public health impact than clinic-based testing, and that enhanced linkage strategies will amplify these differences Overall, our findings will provide evidence to inform clinical protocols and govern-ment policy regarding the provision of cervical cancer pre-vention strategies and provide a guide for adaptation and evaluation of similar programs in other settings Ultimately programs that both use evidence-based techniques and reach a large proportion of the population will impact the millions of women at risk for cervical cancer in low re-source countries worldwide

Conclusions This project will have broad implications at both local and national policy and planning levels, given the enthusiasm of the Kenya Ministry of Health and Division of Reproductive Health to implement na-tional cervical cancer prevention strategies and their partnership in this project When the analyses are complete, we will have produced a comprehensive de-scription of barriers and facilitators to providing clinic and community-based cervical cancer screening through HPV testing, determined which strategy has greater reach and a better cost-effectiveness profile, and developed a strategy to improve linkage to treatment in partnership with the community If a community-based screening strategy is shown to have more reach with a favorable cost-effectiveness profile, this could be a viable strategy for roll-out in similar settings in Kenya and possibly for adap-tation to other East African countries with a high cervical cancer burdens Just as importantly, if community-based testing is more effective and scalable than clinic-based testing, we will explore factors necessary to improve access to clinic for cervical cancer screening and other preventive care services

Fig 3 Quantitative process measures for four aspects of cervical cancer prevention program delivery

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